The highly buffered Arabidopsis immune signaling network conceals the functions of its components

Rachel A. Hillmer, Kenichi Tsuda, Ghanasyam Rallapalli, Shuta Asai, William Truman, Matthew D. Papke, Hitoshi Sakakibara, Jonathan D.G. Jones, Chad L Myers, Fumiaki Katagiri

Research output: Contribution to journalArticlepeer-review

62 Scopus citations

Abstract

Plant immunity protects plants from numerous potentially pathogenic microbes. The biological network that controls plant inducible immunity must function effectively even when network components are targeted and disabled by pathogen effectors. Network buffering could confer this resilience by allowing different parts of the network to compensate for loss of one another’s functions. Networks rich in buffering rely on interactions within the network, but these mechanisms are difficult to study by simple genetic means. Through a network reconstitution strategy, in which we disassemble and stepwise reassemble the plant immune network that mediates Pattern-Triggered-Immunity, we have resolved systems-level regulatory mechanisms underlying the Arabidopsis transcriptome response to the immune stimulant flagellin-22 (flg22). These mechanisms show widespread evidence of interactions among major sub-networks—we call these sectors—in the flg22-responsive transcriptome. Many of these interactions result in network buffering. Resolved regulatory mechanisms show unexpected patterns for how the jasmonate (JA), ethylene (ET), phytoalexin-deficient 4 (PAD4), and salicylate (SA) signaling sectors control the transcriptional response to flg22. We demonstrate that many of the regulatory mechanisms we resolved are not detectable by the traditional genetic approach of single-gene null-mutant analysis. Similar to potential pathogenic perturbations, null-mutant effects on immune signaling can be buffered by the network.

Original languageEnglish (US)
Article numbere1006639
JournalPLoS genetics
Volume13
Issue number5
DOIs
StatePublished - May 2017

Bibliographical note

Publisher Copyright:
© 2017 Hillmer et al.

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